Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues

Abstract

The circadian clock increases organisms' fitness by regulating physiological responses1. In mammals, the circadian clock in the suprachiasmatic nucleus (SCN) governs daily behavioural rhythms2. Similarly, in Arabidopsis, tissue-specific circadian clock functions have emerged, and the importance of the vasculature clock for photoperiodic flowering has been demonstrated. However, it remains unclear if the vasculature clock regulates the majority of physiological responses, like the SCN in mammals, and if other environmental signals are also processed by the vasculature clock. Here, we studied the involvement of tissue-specific circadian clock regulation of flowering and cell elongation under different photoperiods and temperatures. We found that the circadian clock in vascular phloem companion cells is essential for photoperiodic flowering regulation; by contrast, the epidermis has a crucial impact on ambient temperature-dependent cell elongation. Thus, there are clear assignments of roles among circadian clocks in each tissue. Our results reveal that, unlike the more centralized circadian clock in mammals, the plant circadian clock is decentralized, where each tissue specifically processes individual environmental cues and regulates individual physiological responses. Our new conceptual framework will be a starting point for deciphering circadian clock functions in each tissue, which will lead to a better understanding of how circadian clock processing of environmental signals may be affected by ongoing climate change.